XB-ART-49454
Dev Dyn
December 1, 2014;
243
(12):
1606-18.
Early stages of induction of anterior head ectodermal properties in Xenopus embryos are mediated by transcriptional cofactor ldb1.
Plautz CZ
,
Zirkle BE
,
Deshotel MJ
,
Grainger RM
.
Abstract
Specific molecules involved in early inductive signaling from anterior neural tissue to the placodal ectoderm to establish a lens-forming bias, as well as their regulatory factors, remain largely unknown. In this study, we sought to identify and characterize these molecules. Using an expression cloning strategy to isolate genes with lens-inducing activity, we identified the transcriptional cofactor ldb1. This, together with evidence for its nuclear dependence, suggests its role as a regulatory factor, not a direct signaling molecule. We propose that ldb1 mediates induction of early lens genes in our functional assay by transcriptional activation of lens-inducing signals. Gain-of-function assays demonstrate that the inductive activity of the anterior neural plate on head ectodermal structures can be augmented by ldb1. Loss-of-function assays show that knockdown of ldb1 leads to decreased expression of early lens and retinal markers and subsequently to defects in eye development. The functional cloning, expression pattern, overexpression, and knockdown data show that an ldb1-regulated mechanism acts as an early signal for Xenopus lens induction.
PubMed ID: 25258326
PMC ID: PMC4237673
Article link: Dev Dyn
Grant support: [+]
R01 EY006675 NEI NIH HHS , R01 EY010283 NEI NIH HHS , R01 EY017400 NEI NIH HHS , EY05542 NEI NIH HHS , EY06675 NEI NIH HHS , EY10283 NEI NIH HHS , EY17400 NEI NIH HHS , R01 EY022954 NEI NIH HHS
Species referenced: Xenopus
Genes referenced: ag1 dll1 dlx5 foxe3 ldb1 ldb2 maf nrl rax
Morpholinos: ldb1 MO1
Article Images: [+] show captions
References [+] :
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Interactions of the LIM-domain-binding factor Ldb1 with LIM homeodomain proteins.
1996, Pubmed,
Xenbase
Agulnick,
Interactions of the LIM-domain-binding factor Ldb1 with LIM homeodomain proteins.
1996,
Pubmed
,
Xenbase
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Baker, Vertebrate cranial placodes I. Embryonic induction. 2001, Pubmed , Xenbase
Bhattacharyya, Clonal analyses in the anterior pre-placodal region: implications for the early lineage bias of placodal progenitors. 2014, Pubmed
Chitnis, Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. 1995, Pubmed , Xenbase
Chomczynski, Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. 1987, Pubmed
Cross, LIM domain binding proteins 1 and 2 have different oligomeric states. 2010, Pubmed
Dabauvalle, Role of nuclear material in the early cell cycle of Xenopus embryos. 1988, Pubmed , Xenbase
Deng, Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor. 2012, Pubmed
Drysdale, Inductive events in the patterning of the Xenopus laevis hatching and cement glands, two cell types which delimit head boundaries. 1993, Pubmed , Xenbase
Eagleson, Mapping of the presumptive brain regions in the neural plate of Xenopus laevis. 1990, Pubmed , Xenbase
Fini, Perspectives on eye development. 1997, Pubmed , Xenbase
Gallagher, Inductive processes leading to inner ear formation during Xenopus development. 1996, Pubmed , Xenbase
Gammill, Identification of otx2 target genes and restrictions in ectodermal competence during Xenopus cement gland formation. 1997, Pubmed , Xenbase
Gans, Neural crest and the origin of vertebrates: a new head. 2010, Pubmed
Grainger, Embryonic lens induction: shedding light on vertebrate tissue determination. 1993, Pubmed , Xenbase
Grainger, Defining intermediate stages in cell determination: acquisition of a lens-forming bias in head ectoderm during lens determination. 1997, Pubmed , Xenbase
Güngör, Proteasomal selection of multiprotein complexes recruited by LIM homeodomain transcription factors. 2007, Pubmed
Henry, Early tissue interactions leading to embryonic lens formation in Xenopus laevis. 1990, Pubmed , Xenbase
Hiratani, Selective degradation of excess Ldb1 by Rnf12/RLIM confers proper Ldb1 expression levels and Xlim-1/Ldb1 stoichiometry in Xenopus organizer functions. 2003, Pubmed , Xenbase
Howard, Transcription intermediary factor 1gamma decreases protein expression of the transcriptional cofactor, LIM-domain-binding 1. 2010, Pubmed
Howard, Regulation of LIM-domain-binding 1 protein expression by ubiquitination of Lys134. 2010, Pubmed , Xenbase
Hwang, The neuronal differentiation potential of Ldb1-null mutant embryonic stem cells is dependent on extrinsic influences. 2008, Pubmed
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Krivega, Role of LDB1 in the transition from chromatin looping to transcription activation. 2014, Pubmed
Li, Nuclear adaptor Ldb1 regulates a transcriptional program essential for the maintenance of hematopoietic stem cells. 2011, Pubmed
Lustig, Use of an oocyte expression assay to reconstitute inductive signaling. 1995, Pubmed , Xenbase
Matthews, LIM-domain-binding protein 1: a multifunctional cofactor that interacts with diverse proteins. 2003, Pubmed
Matthews, Competition between LIM-binding domains. 2008, Pubmed
Mayor, Induction of the prospective neural crest of Xenopus. 1995, Pubmed , Xenbase
Medina-Martinez, Foxe view of lens development and disease. 2007, Pubmed , Xenbase
Meier, Novel binding partners of Ldb1 are required for haematopoietic development. 2006, Pubmed
Miazga, Coordinating the timing of cardiac precursor development during gastrulation: a new role for Notch signaling. 2009, Pubmed , Xenbase
Mizuseki, Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction. 1998, Pubmed , Xenbase
Mochizuki, Xlim-1 and LIM domain binding protein 1 cooperate with various transcription factors in the regulation of the goosecoid promoter. 2000, Pubmed , Xenbase
Mukhopadhyay, Functional ablation of the mouse Ldb1 gene results in severe patterning defects during gastrulation. 2002, Pubmed
Ogino, Sequential activation of transcription factors in lens induction. 2001, Pubmed , Xenbase
Ogino, Convergence of a head-field selector Otx2 and Notch signaling: a mechanism for lens specification. 2007, Pubmed , Xenbase
Ogino, [Involvement of maf gene family in crystallin gene regulation]. 1997, Pubmed
Ostendorff, Dynamic expression of LIM cofactors in the developing mouse neural tube. 2006, Pubmed
Pandit, BMP-induced L-Maf regulates subsequent BMP-independent differentiation of primary lens fibre cells. 2011, Pubmed
Pannese, The Xenopus homologue of Otx2 is a maternal homeobox gene that demarcates and specifies anterior body regions. 1995, Pubmed , Xenbase
Papalopulu, Xenopus Distal-less related homeobox genes are expressed in the developing forebrain and are induced by planar signals. 1993, Pubmed , Xenbase
Schlosser, Induction and specification of cranial placodes. 2006, Pubmed , Xenbase
Schlosser, Molecular anatomy of placode development in Xenopus laevis. 2004, Pubmed , Xenbase
Schlosser, Eya1 and Six1 promote neurogenesis in the cranial placodes in a SoxB1-dependent fashion. 2008, Pubmed , Xenbase
Servetnick, Changes in neural and lens competence in Xenopus ectoderm: evidence for an autonomous developmental timer. 1992, Pubmed , Xenbase
Sive, Progressive determination during formation of the anteroposterior axis in Xenopus laevis. 1989, Pubmed , Xenbase
Slack, Regional biosynthetic markers in the early amphibian embryo. 1984, Pubmed
Smith, Injected Xwnt-8 RNA acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center. 1991, Pubmed , Xenbase
Smith, Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. 1992, Pubmed , Xenbase
Smolich, Characterization of Xenopus laevis gamma-crystallin-encoding genes. 1993, Pubmed , Xenbase
Sokol, Injected Wnt RNA induces a complete body axis in Xenopus embryos. 1991, Pubmed , Xenbase
Song, Multiple functions of Ldb1 required for beta-globin activation during erythroid differentiation. 2010, Pubmed
Teufel, Liver-specific Ldb1 deletion results in enhanced liver cancer development. 2010, Pubmed
Tzchori, LIM homeobox transcription factors integrate signaling events that control three-dimensional limb patterning and growth. 2009, Pubmed
Viczian, Expression of Xenopus laevis Lhx2 during eye development and evidence for divergent expression among vertebrates. 2006, Pubmed , Xenbase
Wylie, Maternal beta-catenin establishes a 'dorsal signal' in early Xenopus embryos. 1996, Pubmed , Xenbase
Zhao, LIM-homeodomain proteins Lhx1 and Lhx5, and their cofactor Ldb1, control Purkinje cell differentiation in the developing cerebellum. 2007, Pubmed
Zuber, Specification of the vertebrate eye by a network of eye field transcription factors. 2003, Pubmed , Xenbase
Zygar, Gene activation during early stages of lens induction in Xenopus. 1998, Pubmed , Xenbase
de la Calle-Mustienes, Xenopus Xlmo4 is a GATA cofactor during ventral mesoderm formation and regulates Ldb1 availability at the dorsal mesoderm and the neural plate. 2003, Pubmed , Xenbase
Andreazzoli, Role of Xrx1 in Xenopus eye and anterior brain development. 1999, Pubmed , Xenbase
Bach, A family of LIM domain-associated cofactors confer transcriptional synergism between LIM and Otx homeodomain proteins. 1997, Pubmed
Bailey, Regulation of vertebrate eye development by Rx genes. 2004, Pubmed , Xenbase
Baker, Vertebrate cranial placodes I. Embryonic induction. 2001, Pubmed , Xenbase
Bhattacharyya, Clonal analyses in the anterior pre-placodal region: implications for the early lineage bias of placodal progenitors. 2014, Pubmed
Chitnis, Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. 1995, Pubmed , Xenbase
Chomczynski, Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. 1987, Pubmed
Cross, LIM domain binding proteins 1 and 2 have different oligomeric states. 2010, Pubmed
Dabauvalle, Role of nuclear material in the early cell cycle of Xenopus embryos. 1988, Pubmed , Xenbase
Deng, Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor. 2012, Pubmed
Drysdale, Inductive events in the patterning of the Xenopus laevis hatching and cement glands, two cell types which delimit head boundaries. 1993, Pubmed , Xenbase
Eagleson, Mapping of the presumptive brain regions in the neural plate of Xenopus laevis. 1990, Pubmed , Xenbase
Fini, Perspectives on eye development. 1997, Pubmed , Xenbase
Gallagher, Inductive processes leading to inner ear formation during Xenopus development. 1996, Pubmed , Xenbase
Gammill, Identification of otx2 target genes and restrictions in ectodermal competence during Xenopus cement gland formation. 1997, Pubmed , Xenbase
Gans, Neural crest and the origin of vertebrates: a new head. 2010, Pubmed
Grainger, Embryonic lens induction: shedding light on vertebrate tissue determination. 1993, Pubmed , Xenbase
Grainger, Defining intermediate stages in cell determination: acquisition of a lens-forming bias in head ectoderm during lens determination. 1997, Pubmed , Xenbase
Güngör, Proteasomal selection of multiprotein complexes recruited by LIM homeodomain transcription factors. 2007, Pubmed
Henry, Early tissue interactions leading to embryonic lens formation in Xenopus laevis. 1990, Pubmed , Xenbase
Hiratani, Selective degradation of excess Ldb1 by Rnf12/RLIM confers proper Ldb1 expression levels and Xlim-1/Ldb1 stoichiometry in Xenopus organizer functions. 2003, Pubmed , Xenbase
Howard, Transcription intermediary factor 1gamma decreases protein expression of the transcriptional cofactor, LIM-domain-binding 1. 2010, Pubmed
Howard, Regulation of LIM-domain-binding 1 protein expression by ubiquitination of Lys134. 2010, Pubmed , Xenbase
Hwang, The neuronal differentiation potential of Ldb1-null mutant embryonic stem cells is dependent on extrinsic influences. 2008, Pubmed
JACOBSON, THE DETERMINATION AND POSITIONING OF THE NOSE, LENS AND EAR. II. THE ROLE OF THE ENDODERM. 1964, Pubmed
JACOBSON, THE DETERMINATION AND POSITIONING OF THE NOSE, LENS AND EAR. I. INTERACTIONS WITHIN THE ECTODERM, AND BETWEEN THE ECTODERM AND UNDERLYING TISSUES. 1964, Pubmed
Jacobson, Inductive processes in embryonic development. 1966, Pubmed
Jurata, Functional analysis of the nuclear LIM domain interactor NLI. 1997, Pubmed
Kao, The entire mesodermal mantle behaves as Spemann's organizer in dorsoanterior enhanced Xenopus laevis embryos. 1988, Pubmed , Xenbase
Kenyon, A novel fork head gene mediates early steps during Xenopus lens formation. 1999, Pubmed , Xenbase
Kintner, Expression of Xenopus N-CAM RNA in ectoderm is an early response to neural induction. 1987, Pubmed , Xenbase
Kintner, Monoclonal antibodies identify blastemal cells derived from dedifferentiating limb regeneration. 1984, Pubmed , Xenbase
Krivega, Role of LDB1 in the transition from chromatin looping to transcription activation. 2014, Pubmed
Li, Nuclear adaptor Ldb1 regulates a transcriptional program essential for the maintenance of hematopoietic stem cells. 2011, Pubmed
Lustig, Use of an oocyte expression assay to reconstitute inductive signaling. 1995, Pubmed , Xenbase
Matthews, LIM-domain-binding protein 1: a multifunctional cofactor that interacts with diverse proteins. 2003, Pubmed
Matthews, Competition between LIM-binding domains. 2008, Pubmed
Mayor, Induction of the prospective neural crest of Xenopus. 1995, Pubmed , Xenbase
Medina-Martinez, Foxe view of lens development and disease. 2007, Pubmed , Xenbase
Meier, Novel binding partners of Ldb1 are required for haematopoietic development. 2006, Pubmed
Miazga, Coordinating the timing of cardiac precursor development during gastrulation: a new role for Notch signaling. 2009, Pubmed , Xenbase
Mizuseki, Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction. 1998, Pubmed , Xenbase
Mochizuki, Xlim-1 and LIM domain binding protein 1 cooperate with various transcription factors in the regulation of the goosecoid promoter. 2000, Pubmed , Xenbase
Mukhopadhyay, Functional ablation of the mouse Ldb1 gene results in severe patterning defects during gastrulation. 2002, Pubmed
Ogino, Sequential activation of transcription factors in lens induction. 2001, Pubmed , Xenbase
Ogino, Convergence of a head-field selector Otx2 and Notch signaling: a mechanism for lens specification. 2007, Pubmed , Xenbase
Ogino, [Involvement of maf gene family in crystallin gene regulation]. 1997, Pubmed
Ostendorff, Dynamic expression of LIM cofactors in the developing mouse neural tube. 2006, Pubmed
Pandit, BMP-induced L-Maf regulates subsequent BMP-independent differentiation of primary lens fibre cells. 2011, Pubmed
Pannese, The Xenopus homologue of Otx2 is a maternal homeobox gene that demarcates and specifies anterior body regions. 1995, Pubmed , Xenbase
Papalopulu, Xenopus Distal-less related homeobox genes are expressed in the developing forebrain and are induced by planar signals. 1993, Pubmed , Xenbase
Schlosser, Induction and specification of cranial placodes. 2006, Pubmed , Xenbase
Schlosser, Molecular anatomy of placode development in Xenopus laevis. 2004, Pubmed , Xenbase
Schlosser, Eya1 and Six1 promote neurogenesis in the cranial placodes in a SoxB1-dependent fashion. 2008, Pubmed , Xenbase
Servetnick, Changes in neural and lens competence in Xenopus ectoderm: evidence for an autonomous developmental timer. 1992, Pubmed , Xenbase
Sive, Progressive determination during formation of the anteroposterior axis in Xenopus laevis. 1989, Pubmed , Xenbase
Slack, Regional biosynthetic markers in the early amphibian embryo. 1984, Pubmed
Smith, Injected Xwnt-8 RNA acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center. 1991, Pubmed , Xenbase
Smith, Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. 1992, Pubmed , Xenbase
Smolich, Characterization of Xenopus laevis gamma-crystallin-encoding genes. 1993, Pubmed , Xenbase
Sokol, Injected Wnt RNA induces a complete body axis in Xenopus embryos. 1991, Pubmed , Xenbase
Song, Multiple functions of Ldb1 required for beta-globin activation during erythroid differentiation. 2010, Pubmed
Teufel, Liver-specific Ldb1 deletion results in enhanced liver cancer development. 2010, Pubmed
Tzchori, LIM homeobox transcription factors integrate signaling events that control three-dimensional limb patterning and growth. 2009, Pubmed
Viczian, Expression of Xenopus laevis Lhx2 during eye development and evidence for divergent expression among vertebrates. 2006, Pubmed , Xenbase
Wylie, Maternal beta-catenin establishes a 'dorsal signal' in early Xenopus embryos. 1996, Pubmed , Xenbase
Zhao, LIM-homeodomain proteins Lhx1 and Lhx5, and their cofactor Ldb1, control Purkinje cell differentiation in the developing cerebellum. 2007, Pubmed
Zuber, Specification of the vertebrate eye by a network of eye field transcription factors. 2003, Pubmed , Xenbase
Zygar, Gene activation during early stages of lens induction in Xenopus. 1998, Pubmed , Xenbase
de la Calle-Mustienes, Xenopus Xlmo4 is a GATA cofactor during ventral mesoderm formation and regulates Ldb1 availability at the dorsal mesoderm and the neural plate. 2003, Pubmed , Xenbase